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Salmo Trutta) in Britain and Ireland: Glacial Refugia, Post-Glacial Colonisation, and Origins of Sympatric Populations Mckeown, N., Hynes, R., Duguid, R

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Salmo Trutta) in Britain and Ireland: Glacial Refugia, Post-Glacial Colonisation, and Origins of Sympatric Populations Mckeown, N., Hynes, R., Duguid, R Phylogeographic structure of brown trout (Salmo trutta) in Britain and Ireland: glacial refugia, post-glacial colonisation, and origins of sympatric populations McKeown, N., Hynes, R., Duguid, R. A., Ferguson, A., & Prodöhl, P. (2010). Phylogeographic structure of brown trout (Salmo trutta) in Britain and Ireland: glacial refugia, post-glacial colonisation, and origins of sympatric populations. Journal of Fish Biology, 76(2), 319-347. https://doi.org/10.1111/j.1095-8649.2009.02490.x Published in: Journal of Fish Biology Queen's University Belfast - Research Portal: Link to publication record in Queen's University Belfast Research Portal General rights Copyright for the publications made accessible via the Queen's University Belfast Research Portal is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policy The Research Portal is Queen's institutional repository that provides access to Queen's research output. Every effort has been made to ensure that content in the Research Portal does not infringe any person's rights, or applicable UK laws. If you discover content in the Research Portal that you believe breaches copyright or violates any law, please contact [email protected]. Download date:01. Oct. 2021 Journal of Fish Biology (2010) 76, 319–347 doi:10.1111/j.1095-8649.2009.02490.x, available online at www.interscience.wiley.com Phylogeographic structure of brown trout Salmo trutta in Britain and Ireland: glacial refugia, postglacial colonization and origins of sympatric populations N.J.McKeown*,R.A.Hynes,R.A.Duguid†,A.Ferguson and P. A. Prodohl‡¨ School of Biological Sciences, Queen’s University Belfast, MBC 97 Lisburn Road, Belfast BT9 7BL, Northern Ireland, U.K. (Received 15 March 2009, Accepted 13 October 2009) The phylogeographical structure of brown trout Salmo trutta in Britain and Ireland was studied using polymerase chain reaction–restriction fragment length polymorphism (PCR–RFLP) analysis of four mitochondrial DNA segments (16S/ND1, ND5/6, COXIII/ND5 and ND5/12S). Analysis of 3636 individuals from 83 sites–morphotypes revealed a total of 25 haplotypes. These haplotypes were nested in seven two-step clades. Although there was a clear geographical patterning to the occurrence of derived clades, admixture among ancestral clades was extensive throughout the studied area. A relevant feature of the data was that some populations contained mixtures of highly divergent clades. This type II phylogeographic pattern is uncommon in nature. Clade intermixing is likely to have taken place during earlier interglacials as well as since the Last Glacial Maximum. The anadromous life history of many S. trutta populations has probably also contributed to clade mixing. Based on the data presented here and published data, postglacial colonization of Britain and Ireland most likely involved S. trutta from at least five potential glacial refuges. Probable locations for such refugia were: south of England–western France, east of the Baltic Sea, western Ireland, Celtic Sea and North Sea. Ferox S. trutta, as defined by their longevity, late maturation and piscivory, exhibited a strong association with a particular clade indicating that they share a common ancestor. Current evidence indicates that the Lough Melvin gillaroo S. trutta and sonaghen S. trutta sympatric types diverged prior to colonization of Lough Melvin and, although limited gene flow has occurred since secondary contact, they have remained largely reproductively isolated due to inlet and outlet river spawning segregation. Gillaroo S. trutta may reflect descendents of a previously more widespread lineage that has declined due to habitat alterations particularly affecting outlet rivers. The mosaic-like distribution of mtDNA lineages means that conservation prioritization in Britain and Ireland should be based on the biological characteristics of local populations rather than solely on evolutionary lineages. © 2010 The Authors Journal compilation © 2010 The Fisheries Society of the British Isles Key words: brown trout; mitochondrial DNA; PCR–RFLP; phylogeography; sympatric populations. ‡Author to whom correspondence should be addressed. Tel.: + 44 2890 972267; email: [email protected] *Present address: School of Biological Science, Royal Holloway University of London, Surrey, TW20 0EX, England, U.K. †Present address: Scottish Environment Protection Agency, 7 Whitefriars Crescent, Perth, PH2 0 PA, Scotland, U.K. 319 © 2010 The Authors Journal compilation © 2010 The Fisheries Society of the British Isles 320 N. J. MCKEOWN ET AL. INTRODUCTION The brown trout Salmo trutta L. displays extensive genetic, ecological, morphologi- cal and life-history variation (Ferguson, 1989), which has resulted in a long-standing debate on the evolutionary origins and taxonomic implications of this variability (Gunther,¨ 1866; Behnke, 1972; Kottelat & Freyhof, 2007). The Atlantic group (sensu Bernatchez, 2001) of S. trutta is currently distributed from Morocco northwards to Iceland, together with the Baltic and White Seas. Based on the degree of mitochon- drial DNA (mtDNA) divergence, Bernatchez (2001) suggested that this group split from the more eastern S. trutta groups during the early to mid-Pleistocene, some 700 000 years before present (b.p.). In NW Europe, this period since separation of the Atlantic group encompasses major climatic oscillations that resulted in several glacial and interglacial periods (Webb & Bartlein, 1992; Clark et al., 2004). Many studies of fish and other organisms have revealed the dramatic effects of these Pleis- tocene glaciations on evolution and current distribution of species (Hewitt, 2004). The most recent glacial period started c. 30 000 b.p. and reached a maximum (Last Glacial Maximum, LGM) some 23 000 to 18 000 b.p. (Bowen et al., 2002; Clark et al., 2004; Knight et al., 2004). During the LGM ice covered much of Britain and Ireland, although some periph- eral regions such as the south and west of Ireland, and south of England remained free from glaciation (Clark et al., 2004). In addition, as a result of the lowered sea level, the land mass was considerably extended in comparison with today (Clark et al., 2004), providing possible refugia in areas that are currently marine. Salmo trutta is potentially anadromous and this would have allowed both rapid range retreat into refugia during glacial periods and subsequent expansion during inter- glacial periods. Similarly, the sea would not have presented a barrier to postglacial colonization of current freshwater catchments. Thus, most, if not all, native S. trutta populations in Britain and Ireland, irrespective of current life history, colonized as anadromous S. trutta (Ferguson, 2006). Anadromy has allowed continued gene flow between populations in some adjacent catchments. These interlinked factors sug- gest that the phylogeographic structure of S. trutta in NW Europe is likely to be more complex than that described for many other organisms. Overall, there have been repeated opportunities for genetic divergence in allopatric refuges, followed by interbreeding, or varying degrees of reproductive isolation, on secondary contact after postglacial colonization. This prediction is supported by studies of S. trutta that have revealed a complex phylogeographic structure within NW Europe. Although the consensus is that postglacial colonization involved multiple lineages originating from separate refuges, hypotheses differ in terms of the number, origin and disper- sal dynamics of these lineages (Ferguson & Fleming, 1983; Hamilton et al., 1989; Hynes et al., 1996; Garc´ıa-Mar´ın et al., 1999; Weiss et al., 2000; Bernatchez, 2001; Cortey et al., 2009). More extensive sampling and increased phylogeographic reso- lution are therefore necessary to clarify the evolutionary history of S. trutta in this region, especially given that, to date, only limited studies have been undertaken in Britain and Ireland. In several waters throughout the range of the species, two or more populations of S. trutta have been found to co-occur (Allendorf et al., 1976; Ferguson & Mason, 1981; Crozier & Ferguson, 1986; Susnikˇ et al., 2005; Duguid et al., 2006). Typically these sympatric populations show significant interpopulation differences in allele © 2010 The Authors Journal compilation © 2010 The Fisheries Society of the British Isles, Journal of Fish Biology 2010, 76, 319–347 PHYLOGEOGRAPHY OF SALMO TRUTTA FROM NW EUROPE 321 frequencies and, since only limited gene flow is necessary to result in homogeneity of neutral alleles (Morjan & Rieseberg, 2004), a high degree of reproductive isolation must be present. One of the best studied examples is the sympatric gillaroo S. trutta, sonaghen S. trutta and ferox S. trutta populations in Lough Melvin, NW Ireland (reviewed by Ferguson, 2004). Based on their genetic, morphological and ecological differentiation (Ferguson & Mason, 1981; Ferguson, 1986; Cawdery & Ferguson, 1988; Ferguson & Taggart, 1991; Prodohl,¨ 1993; McVeigh et al., 1995), and to highlight their conservation importance, Ferguson (2004) considered these as distinct biological species. He proposed reinstatement of the 19th century scientific names of gillaroo Salmo stomachicus Gunther,¨ sonaghen Salmo nigripinnis Gunther¨ and ferox Salmo ferox Jardine. This classification is also used by Kottelat & Freyhof (2007). A fuller understanding of the evolutionary origins and homologies to
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